Micellization: A new principle in the formation of biomolecular condensates

Phase separation is a fundamental mechanism for compartmentalization in cells and leads to the formation of biomolecular condensates, generally containing various RNA molecules. RNAs are biomolecules that can serve as suitable scaffolds for biomolecular condensates and determine their forms and functions. Many studies have focused on biomolecular condensates formed by liquid-liquid phase separation (LLPS), one type of intracellular phase separation mechanism. We recently identified that paraspeckle nuclear bodies use an intracellular phase separation mechanism called micellization of block copolymers in their formation. The paraspeckles are scaffolded by NEAT1_2 long non-coding RNAs (lncRNAs) and their partner RNA-binding proteins (NEAT1_2 RNA-protein complexes [RNPs]). The NEAT1_2 RNPs act as block copolymers and the paraspeckles assemble through micellization. In LLPS, condensates grow without bound as long as components are available and typically have spherical shapes to minimize surface tension. In contrast, the size, shape, and internal morphology of the condensates are more strictly controlled in micellization. Here, we discuss the potential importance and future perspectives of micellization of block copolymers of RNPs in cells, including the construction of designer condensates with optimal internal organization, shape, and size according to design guidelines of block copolymers.

[1]  Jesse M. Platt,et al.  Genetic variation associated with condensate dysregulation in disease. , 2022, Developmental cell.

[2]  R. Pappu,et al.  A conceptual framework for understanding phase separation and addressing open questions and challenges. , 2022, Molecular cell.

[3]  R. Parker,et al.  RNA is required for the integrity of multiple nuclear and cytoplasmic membrane‐less RNP granules , 2022, The EMBO journal.

[4]  Yoshimi Kawamura,et al.  Species-specific formation of paraspeckles in intestinal epithelium revealed by characterization of NEAT1 in naked mole-rat , 2022, bioRxiv.

[5]  R. Young,et al.  RNA in formation and regulation of transcriptional condensates , 2021, RNA.

[6]  E. Makeyev,et al.  Hybridization-proximity labeling reveals spatially ordered interactions of nuclear RNA compartments , 2021, Molecular cell.

[7]  C. Brangwynne,et al.  Phase separation vs aggregation behavior for model disordered proteins. , 2021, The Journal of chemical physics.

[8]  A. Gladfelter,et al.  Getting droplets into shape , 2021, Science.

[9]  Chiu Fan Lee,et al.  Regulation of biomolecular condensates by interfacial protein clusters , 2021, Science.

[10]  T. Hirose,et al.  Nascent ribosomal RNA acts as surfactant that suppresses growth of fibrillar centers in nucleolus , 2021 .

[11]  A. Yamashita,et al.  Distinct RNA polymerase transcripts direct the assembly of phase-separated DBC1 nuclear bodies in different cell lines , 2021, Molecular biology of the cell.

[12]  T. Jensen,et al.  hnRNPH1-MTR4 complex-mediated regulation of NEAT1v2 stability is critical for IL8 expression , 2021, RNA biology.

[13]  Michael J. Bolt,et al.  Enhancer RNA m6A methylation facilitates transcriptional condensate formation and gene activation. , 2021, Molecular cell.

[14]  T. Hirose,et al.  Control of condensates dictates nucleolar architecture , 2021, Science.

[15]  J. Iwakiri,et al.  m6A modification of HSATIII lncRNAs regulates temperature‐dependent splicing , 2021, The EMBO journal.

[16]  J. Mendell,et al.  NORAD-induced Pumilio phase separation is required for genome stability , 2021, Nature.

[17]  Taro Mannen,et al.  ArcRNAs and the formation of nuclear bodies , 2021, Mammalian Genome.

[18]  D. Patel,et al.  N6-Methyladenosine on mRNA facilitates a phase-separated nuclear body that suppresses myeloid leukemic differentiation. , 2021, Cancer cell.

[19]  G. Pierron,et al.  Paraspeckles are constructed as block copolymer micelles , 2021, The EMBO journal.

[20]  Maxwell I. Zimmerman,et al.  The SARS-CoV-2 nucleocapsid protein is dynamic, disordered, and phase separates with RNA , 2021, Nature Communications.

[21]  A. Fox,et al.  Paraspeckle nuclear condensates: Global sensors of cell stress? , 2021, BioEssays : news and reviews in molecular, cellular and developmental biology.

[22]  H. Kimura,et al.  Transcription organizes euchromatin via microphase separation , 2021, Nature Communications.

[23]  J. Diedrich,et al.  The SARS-CoV-2 nucleocapsid phosphoprotein forms mutually exclusive condensates with RNA and the membrane-associated M protein , 2021, Nature Communications.

[24]  M. Rosen,et al.  A framework for understanding the functions of biomolecular condensates across scales , 2020, Nature Reviews Molecular Cell Biology.

[25]  T. Hirose,et al.  Triblock copolymer micelle model of spherical paraspeckles , 2020, bioRxiv.

[26]  A. Fox,et al.  NEAT1 polyA-modulating antisense oligonucleotides reveal opposing functions for both long non-coding RNA isoforms in neuroblastoma , 2020, Cellular and Molecular Life Sciences.

[27]  Joshua A. Riback,et al.  The nucleolus as a multiphase liquid condensate , 2020, Nature Reviews Molecular Cell Biology.

[28]  Nazim Madhavji,et al.  Organization , 2020, WER.

[29]  M. Guttman,et al.  RNA promotes the formation of spatial compartments in the nucleus , 2020, Cell.

[30]  F. Meng,et al.  Modeling Elastically Mediated Liquid-Liquid Phase Separation. , 2020, Physical review letters.

[31]  R. Young,et al.  Biomolecular Condensates in the Nucleus. , 2020, Trends in biochemical sciences.

[32]  R. Pappu,et al.  Restricting the sizes of condensates , 2020, eLife.

[33]  A. Gladfelter,et al.  RNA contributions to the form and function of biomolecular condensates , 2020, Nature Reviews Molecular Cell Biology.

[34]  Chandra L. Theesfeld,et al.  Genomic RNA Elements Drive Phase Separation of the SARS-CoV-2 Nucleocapsid , 2020, Molecular Cell.

[35]  R. Shiekhattar,et al.  Integrator restrains paraspeckles assembly by promoting isoform switching of the lncRNA NEAT1 , 2020, Science Advances.

[36]  M. Zweckstetter,et al.  Nucleocapsid protein of SARS-CoV-2 phase separates into RNA-rich polymerase-containing condensates , 2020, Nature Communications.

[37]  E. Shakhnovich,et al.  Dynamic metastable long-living droplets formed by sticker-spacer proteins , 2020, eLife.

[38]  Z. Songyang,et al.  Live cell imaging and proteomic profiling of endogenous NEAT1 lncRNA by CRISPR/Cas9-mediated knock-in , 2020, Protein & Cell.

[39]  T. Hirose,et al.  Phase separation driven by production of architectural RNA transcripts. , 2020, Soft matter.

[40]  Shunmin He,et al.  RIC-seq for global in situ profiling of RNA–RNA spatial interactions , 2020, Nature.

[41]  Y. Hiraoka Phase separation drives pairing of homologous chromosomes , 2020, Current Genetics.

[42]  Joshua A. Riback,et al.  Competing Protein-RNA Interaction Networks Control Multiphase Intracellular Organization , 2020, Cell.

[43]  Hong Joo Kim,et al.  G3BP1 Is a Tunable Switch that Triggers Phase Separation to Assemble Stress Granules , 2020, Cell.

[44]  R. Pappu,et al.  RNA-Induced Conformational Switching and Clustering of G3BP Drive Stress Granule Assembly by Condensation , 2020, Cell.

[45]  S. Akira,et al.  Dysregulated Expression of the Nuclear Exosome Targeting Complex Component Rbm7 in Nonhematopoietic Cells Licenses the Development of Fibrosis. , 2020, Immunity.

[46]  T. Hirose,et al.  Short Tandem Repeat-Enriched Architectural RNAs in Nuclear Bodies: Functions and Associated Diseases , 2020, Non-coding RNA.

[47]  R. Pappu,et al.  Valence and patterning of aromatic residues determine the phase behavior of prion-like domains , 2020, Science.

[48]  S. Nakagawa,et al.  Architectural RNAs for Membraneless Nuclear Body Formation. , 2020, Cold Spring Harbor symposia on quantitative biology.

[49]  Jun Yu,et al.  Analyses of non-coding somatic drivers in 2,658 cancer whole genomes , 2020, Nature.

[50]  M. Ohno,et al.  ARS2 Regulates Nuclear Paraspeckle Formation through 3′-End Processing and Stability of NEAT1 Long Noncoding RNA , 2019, Molecular and Cellular Biology.

[51]  K. Shirahige,et al.  Chromosome-associated RNA–protein complexes promote pairing of homologous chromosomes during meiosis in Schizosaccharomyces pombe , 2019, Nature Communications.

[52]  Howard Y. Chang,et al.  PIRCh-seq: functional classification of non-coding RNAs associated with distinct histone modifications , 2019, Genome Biology.

[53]  Howard Y. Chang,et al.  PIRCh-seq: functional classification of non-coding RNAs associated with distinct histone modifications , 2019, Genome Biology.

[54]  J. Iwakiri,et al.  LncRNA‐dependent nuclear stress bodies promote intron retention through SR protein phosphorylation , 2019, The EMBO journal.

[55]  W. Robberecht,et al.  RNA toxicity in non‐coding repeat expansion disorders , 2019, The EMBO journal.

[56]  S. Nakagawa,et al.  Molecular anatomy of the architectural NEAT1 noncoding RNA: The domains, interactors, and biogenesis pathway required to build phase‐separated nuclear paraspeckles , 2019, Wiley interdisciplinary reviews. RNA.

[57]  Haiyan An,et al.  Stress granules regulate stress-induced paraspeckle assembly , 2019, The Journal of cell biology.

[58]  Luke E. Berchowitz,et al.  Phase separation in biology and disease—a symposium report , 2019, Annals of the New York Academy of Sciences.

[59]  M. Nakao,et al.  The Eleanor ncRNAs activate the topological domain of the ESR1 locus to balance against apoptosis , 2019, Nature Communications.

[60]  E. Dufresne,et al.  Elastic ripening and inhibition of liquid-liquid phase separation , 2019, Nature physics.

[61]  Christopher J. F. Cameron,et al.  RADICL-seq identifies general and cell type–specific principles of genome-wide RNA-chromatin interactions , 2019, Nature Communications.

[62]  J. Yates,et al.  RNA promotes phase separation of glycolysis enzymes into yeast G bodies in hypoxia , 2019, bioRxiv.

[63]  D. Cacchiarelli,et al.  Cross-Regulation between TDP-43 and Paraspeckles Promotes Pluripotency-Differentiation Transition , 2019, Molecular cell.

[64]  S. P. Moran,et al.  lncRNA DIGIT and BRD3 protein form phase-separated condensates to regulate endoderm differentiation , 2019, bioRxiv.

[65]  T. Mittag,et al.  Considerations and Challenges in Studying Liquid-Liquid Phase Separation and Biomolecular Condensates , 2019, Cell.

[66]  I. Costa,et al.  Isolation and genome-wide characterization of cellular DNA:RNA triplex structures , 2019, Nucleic acids research.

[67]  E. Makeyev,et al.  A Short Tandem Repeat-Enriched RNA Assembles a Nuclear Compartment to Control Alternative Splicing and Promote Cell Survival , 2018, Molecular cell.

[68]  Ned S. Wingreen,et al.  Liquid Nuclear Condensates Mechanically Sense and Restructure the Genome , 2018, Cell.

[69]  D. Weil,et al.  RNA is a critical element for the sizing and the composition of phase-separated RNA–protein condensates , 2018, Nature Communications.

[70]  Ling-Ling Chen,et al.  Genome-wide screening of NEAT1 regulators reveals cross-regulation between paraspeckles and mitochondria , 2018, Nature Cell Biology.

[71]  R. Parker,et al.  Emerging Roles for Intermolecular RNA-RNA Interactions in RNP Assemblies , 2018, Cell.

[72]  T. Jensen,et al.  Diminished nuclear RNA decay upon Salmonella infection upregulates antibacterial noncoding RNAs , 2018, The EMBO journal.

[73]  C. Bond,et al.  Functional Domains of NEAT1 Architectural lncRNA Induce Paraspeckle Assembly through Phase Separation. , 2018, Molecular cell.

[74]  P. Tomançak,et al.  RNA buffers the phase separation behavior of prion-like RNA binding proteins , 2018, Science.

[75]  R. Pappu,et al.  Tadpole-like Conformations of Huntingtin Exon 1 Are Characterized by Conformational Heterogeneity that Persists regardless of Polyglutamine Length. , 2018, Journal of molecular biology.

[76]  M. Perucho,et al.  A novel long non-coding RNA from NBL2 pericentromeric macrosatellite forms a perinucleolar aggregate structure in colon cancer , 2018, Nucleic acids research.

[77]  C. Brangwynne,et al.  Physical principles of intracellular organization via active and passive phase transitions , 2018, Reports on progress in physics. Physical Society.

[78]  R. Pappu,et al.  Profilin reduces aggregation and phase separation of huntingtin N-terminal fragments by preferentially binding to soluble monomers and oligomers , 2018, The Journal of Biological Chemistry.

[79]  T. Hirose,et al.  Nuclear Bodies Built on Architectural Long Noncoding RNAs: Unifying Principles of Their Construction and Function , 2017, Molecules and cells.

[80]  C. Bond,et al.  Paraspeckles: Where Long Noncoding RNA Meets Phase Separation. , 2017, Trends in biochemical sciences.

[81]  G. Shivashankar,et al.  Damage-induced lncRNAs control the DNA damage response through interaction with DDRNAs at individual double-strand breaks , 2017, Nature Cell Biology.

[82]  Michael V. LeVine,et al.  Notch signalling maintains Hedgehog responsiveness via a Gli-dependent mechanism during spinal cord patterning in zebrafish , 2018, bioRxiv.

[83]  R. Pappu,et al.  Monomeric Huntingtin Exon 1 Has Similar Overall Structural Features for Wild-Type and Pathological Polyglutamine Lengths , 2017, Journal of the American Chemical Society.

[84]  C. Brangwynne,et al.  Liquid phase condensation in cell physiology and disease , 2017, Science.

[85]  E. Dufresne,et al.  Liquid-Liquid Phase Separation in an Elastic Network , 2017, 1709.00500.

[86]  Bing Zhou,et al.  GRID-seq reveals the global RNA-chromatin interactome , 2017, Nature Biotechnology.

[87]  Y. Sasaki,et al.  Long non‐coding RNA NEAT1 is a transcriptional target of p53 and modulates p53‐induced transactivation and tumor‐suppressor function , 2017, International journal of cancer.

[88]  A. Harvey,et al.  Functional dissection of NEAT1 using genome editing reveals substantial localization of the NEAT1_1 isoform outside paraspeckles , 2017, RNA.

[89]  T. Takumi,et al.  Unusual semi‐extractability as a hallmark of nuclear body‐associated architectural noncoding RNAs , 2017, The EMBO journal.

[90]  J. Lawrence,et al.  Demethylated HSATII DNA and HSATII RNA Foci Sequester PRC1 and MeCP2 into Cancer-Specific Nuclear Bodies. , 2017, Cell reports.

[91]  Anthony A. Hyman,et al.  Biomolecular condensates: organizers of cellular biochemistry , 2017, Nature Reviews Molecular Cell Biology.

[92]  Xiaoyi Cao,et al.  Systematic Mapping of RNA-Chromatin Interactions In Vivo , 2017, Current Biology.

[93]  Xiaoyi Cao,et al.  Systematic Mapping of RNA-Chromatin Interactions In Vivo , 2017, Current Biology.

[94]  Jun Zhang,et al.  Unusual Processing Generates SPA LncRNAs that Sequester Multiple RNA Binding Proteins. , 2016, Molecular cell.

[95]  S. Daunert,et al.  Adaptation to Stressors by Systemic Protein Amyloidogenesis. , 2016, Developmental cell.

[96]  R. Kingston,et al.  Structural, super-resolution microscopy analysis of paraspeckle nuclear body organization , 2016, The Journal of cell biology.

[97]  S. Aerts,et al.  p53 induces formation of NEAT1 lncRNA-containing paraspeckles that modulate replication stress response and chemosensitivity , 2016, Nature Medicine.

[98]  N. Goshima,et al.  The Sam68 nuclear body is composed of two RNase-sensitive substructures joined by the adaptor HNRNPL , 2016, The Journal of cell biology.

[99]  Gérard Pierron,et al.  Functional conservation of the lncRNA NEAT1 in the ancestrally diverged marsupial lineage: Evidence for NEAT1 expression and associated paraspeckle assembly during late gestation in the opossum Monodelphis domestica , 2016, RNA biology.

[100]  Diana M. Mitrea,et al.  Coexisting Liquid Phases Underlie Nucleolar Subcompartments , 2016, Cell.

[101]  Erin M. Langdon,et al.  RNA Controls PolyQ Protein Phase Transitions. , 2015, Molecular cell.

[102]  C. Brangwynne,et al.  RNA transcription modulates phase transition-driven nuclear body assembly , 2015, Proceedings of the National Academy of Sciences.

[103]  C. Bond,et al.  Prion-like domains in RNA binding proteins are essential for building subnuclear paraspeckles , 2015, The Journal of cell biology.

[104]  Y. Ohkawa,et al.  SWI/SNF chromatin-remodeling complexes function in noncoding RNA-dependent assembly of nuclear bodies , 2015, Proceedings of the National Academy of Sciences.

[105]  Ye Xu,et al.  Protein arginine methyltransferase CARM1 attenuates the paraspeckle-mediated nuclear retention of mRNAs containing IRAlus , 2015, Genes & development.

[106]  Eiki Takahashi,et al.  The lncRNA Neat1 is required for corpus luteum formation and the establishment of pregnancy in a subpopulation of mice , 2014, Development.

[107]  Shinichi Nakagawa,et al.  The long noncoding RNA Neat1 is required for mammary gland development and lactation , 2014, RNA.

[108]  Jonathan R. McDaniel,et al.  Noncanonical Self-Assembly of Highly Asymmetric Genetically Encoded Polypeptide Amphiphiles into Cylindrical Micelles , 2014, Nano letters.

[109]  Michael Y Tolstorukov,et al.  The long noncoding RNAs NEAT1 and MALAT1 bind active chromatin sites. , 2014, Molecular cell.

[110]  A. Ishizuka,et al.  Formation of nuclear bodies by the lncRNA Gomafu-associating proteins Celf3 and SF1 , 2014, Genes to cells : devoted to molecular & cellular mechanisms.

[111]  Yutaka Suzuki,et al.  Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. , 2014, Molecular cell.

[112]  Takahide Yokoi,et al.  NEAT1 long noncoding RNA regulates transcription via protein sequestration within subnuclear bodies , 2014, Molecular biology of the cell.

[113]  R. Pappu,et al.  Unmasking the roles of N- and C-terminal flanking sequences from exon 1 of huntingtin as modulators of polyglutamine aggregation , 2013, Proceedings of the National Academy of Sciences.

[114]  Dan Liu,et al.  Whole-genome screening identifies proteins localized to distinct nuclear bodies , 2013, The Journal of cell biology.

[115]  H. Okano,et al.  The long non-coding RNA nuclear-enriched abundant transcript 1_2 induces paraspeckle formation in the motor neuron during the early phase of amyotrophic lateral sclerosis , 2013, Molecular Brain.

[116]  Natsuko Miura,et al.  Spatial Reorganization of Saccharomyces cerevisiae Enolase To Alter Carbon Metabolism under Hypoxia , 2013, Eukaryotic Cell.

[117]  Fumiaki Tanaka,et al.  Spliceosome integrity is defective in the motor neuron diseases ALS and SMA , 2013, EMBO molecular medicine.

[118]  J. Steitz,et al.  Formation of triple-helical structures by the 3′-end sequences of MALAT1 and MENβ noncoding RNAs , 2012, Proceedings of the National Academy of Sciences.

[119]  Phillip A Sharp,et al.  A triple helix stabilizes the 3' ends of long noncoding RNAs that lack poly(A) tails. , 2012, Genes & development.

[120]  N. Goshima,et al.  Alternative 3′‐end processing of long noncoding RNA initiates construction of nuclear paraspeckles , 2012, The EMBO journal.

[121]  Yiyong Mai,et al.  Self-assembly of block copolymers. , 2012, Chemical Society reviews.

[122]  C. Bond,et al.  Structure of the heterodimer of human NONO and paraspeckle protein component 1 and analysis of its role in subnuclear body formation , 2012, Proceedings of the National Academy of Sciences.

[123]  R. Piazza Polymer Physics: Applications to Molecular Association and Thermoreversible Gelation , 2012 .

[124]  Timothy P. Lodge,et al.  Multicompartment Block Polymer Micelles , 2012 .

[125]  Marzena Wojciechowska,et al.  Cellular toxicity of expanded RNA repeats: focus on RNA foci , 2011, Human molecular genetics.

[126]  D. Hernandez-Verdun Assembly and disassembly of the nucleolus during the cell cycle , 2011, Nucleus.

[127]  J. Ule,et al.  Characterising the RNA targets and position-dependent splicing regulation by TDP-43; implications for neurodegenerative diseases , 2011, Nature Neuroscience.

[128]  M. Dundr,et al.  Nucleation of nuclear bodies by RNA , 2011, Nature Cell Biology.

[129]  A. Barkan,et al.  Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein , 2010, Proceedings of the National Academy of Sciences.

[130]  D. Spector,et al.  Direct Visualization of the Co-transcriptional Assembly of a Nuclear Body by Noncoding RNAs , 2010, Nature Cell Biology.

[131]  A. Fox,et al.  Highly Ordered Spatial Organization of the Structural Long Noncoding NEAT1 RNAs within Paraspeckle Nuclear Bodies , 2010, Molecular biology of the cell.

[132]  G. Biamonti,et al.  Nuclear stress bodies. , 2010, Cold Spring Harbor perspectives in biology.

[133]  Andreas Vitalis,et al.  Modulation of polyglutamine conformations and dimer formation by the N-terminus of huntingtin. , 2010, Journal of molecular biology.

[134]  G. Carmichael,et al.  Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA. , 2009, Molecular cell.

[135]  A. Hyman,et al.  Germline P Granules Are Liquid Droplets That Localize by Controlled Dissolution/Condensation , 2009, Science.

[136]  John N. Hutchinson,et al.  An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. , 2009, Molecular cell.

[137]  T. Mituyama,et al.  MENε/β noncoding RNAs are essential for structural integrity of nuclear paraspeckles , 2009, Proceedings of the National Academy of Sciences.

[138]  Karl Fischer,et al.  Temperature triggered self-assembly of polypeptides into multivalent spherical micelles. , 2008, Journal of the American Chemical Society.

[139]  Gabriele Varani,et al.  RNA is rarely at a loss for companions; as soon as RNA , 2008 .

[140]  A. Lamond,et al.  P54nrb forms a heterodimer with PSP1 that localizes to paraspeckles in an RNA-dependent manner. , 2005, Molecular biology of the cell.

[141]  M. Rubinstein,et al.  Diblock copolymer micelles in a dilute solution , 2005 .

[142]  Matthias Mann,et al.  Paraspeckles A Novel Nuclear Domain , 2002, Current Biology.

[143]  S. Riva,et al.  Structure and dynamics of hnRNP-labelled nuclear bodies induced by stress treatments. , 2000, Journal of cell science.

[144]  K. Prasanth,et al.  Omega speckles - a novel class of nuclear speckles containing hnRNPs associated with noncoding hsr-omega RNA in Drosophila. , 2000, Journal of cell science.

[145]  G. Fredrickson,et al.  Block Copolymers—Designer Soft Materials , 1999 .

[146]  N. Nukina,et al.  RNA-Assisted Nuclear Transport of the Meiotic Regulator Mei2p in Fission Yeast , 1998, Cell.

[147]  Frank S. Bates,et al.  Origins of Complex Self-Assembly in Block Copolymers , 1996 .

[148]  M. Schick,et al.  Self-assembly of block copolymers , 1996 .

[149]  Rudolf Podgornik,et al.  Statistical thermodynamics of surfaces, interfaces, and membranes , 1995 .

[150]  Schick,et al.  Stable and unstable phases of a diblock copolymer melt. , 1994, Physical review letters.

[151]  J. Bachellerie,et al.  Intranuclear distribution of U1 and U2 snRNAs visualized by high resolution in situ hybridization: revelation of a novel compartment containing U1 but not U2 snRNA in HeLa cells. , 1993, European journal of cell biology.

[152]  A. Halperin,et al.  Polymeric micelles: their relaxation kinetics , 1989 .

[153]  E. Helfand,et al.  Fluctuation effects in the theory of microphase separation in block copolymers , 1987 .

[154]  K. Kawasaki,et al.  Equilibrium morphology of block copolymer melts , 1986 .

[155]  L. Leibler Theory of Microphase Separation in Block Copolymers , 1980 .

[156]  Charles Tanford,et al.  Theory of micelle formation in aqueous solutions , 1974 .

[157]  C. Tanford,et al.  Thermodynamics of micelle formation: prediction of micelle size and size distribution. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[158]  C. Tanford Micelle shape and size , 1972 .

[159]  Erin M. Langdon,et al.  Probing RNA Structure in Liquid-Liquid Phase Separation Using SHAPE-MaP. , 2018, Methods in enzymology.

[160]  Tomohiro Yamazaki Long Noncoding RNAs and Their Applications: Focus on Architectural RNA (arcRNA), a Class of lncRNA , 2018 .

[161]  C. M. Bates,et al.  50th Anniversary Perspective: Block Polymers—Pure Potential , 2017 .

[162]  T. Hirose,et al.  Architectural RNAs (arcRNAs): A class of long noncoding RNAs that function as the scaffold of nuclear bodies. , 2016, Biochimica et biophysica acta.

[163]  T. Hirose,et al.  The building process of the functional paraspeckle with long non-coding RNAs. , 2015, Frontiers in bioscience.

[164]  Daniel S. Bridges,et al.  An Introduction to Polymer Physics , 2009 .

[165]  Paulo P. Amaral,et al.  MEN epsilon/beta nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. , 2009, Genome research.

[166]  Semenov,et al.  Contribution to the theory of microphase layering in block-copolymer melts , 2008 .